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Musical Expertise Is Related to Altered Functional Connectivity During Audiovisual Integration

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Musical Expertise Is Related to Altered Functional Connectivity During Audiovisual Integration Musical expertise is related to altered functional connectivity during audiovisual integration Evangelos Paraskevopoulosa,b, Anja Kraneburgb,c, Sibylle Cornelia Herholzd, Panagiotis D. Bamidisa, and Christo Pantevb,1 aSchool of Medicine, Faculty of Health Sciences, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece; bInstitute for Biomagnetism and Biosignalanalysis, University of Münster, 48149 Münster, Germany; cResearch Group of Chronobiology, Leibniz Research Center for Working Enviroment and Human Factors, Dortmund, 44139 North Rhine-Westphalia, Germany; and dGerman Center for Neurodegenerative Diseases, 53175 Bonn, Germany Edited by Josef P. Rauschecker, Georgetown University, Washington, DC, and accepted by the Editorial Board August 19, 2015 (received for review May 31, 2015) The present study investigated the cortical large-scale functional (8). A recent study by Paraskevopoulos et al. (9) used MEG to network underpinning audiovisual integration via magnetoencepha- reveal the cortical response related to identification of audiovi- lographic recordings. The reorganization of this network related to sual incongruences. These incongruences occurred on the basis long-term musical training was investigated by comparing musicians of an explicitly learned rule, binding otherwise unrelated uni- to nonmusicians. Connectivity was calculated on the basis of the sensory stimuli. The rule was comparable to musical reading: estimated mutual information of the sources’ activity, and the corre- “the higher the position of the circle, the higher the pitch of the sponding networks were statistically compared. Nonmusicians’ re- tone.” We recorded cortical responses to violations of this rule, sults indicated that the cortical network associated with audiovisual to incongruences between expected auditory and visual input. integration supports visuospatial processing and attentional shifting, This response was located in frontotemporal cortical areas. Plas- whereas a sparser network, related to spatial awareness supports the ticity effects related to long-term musical training were investigated identification of audiovisual incongruences. In contrast, musicians’ re- in this cross-sectional study by comparison of musicians and non- sults showed enhanced connectivity in regions related to the identi- musicians, whereas effects of short-term music reading training fication of auditory pattern violations. Hence, nonmusicians rely on were investigated in a follow-up longitudinal study that allowed the processing of visual clues for the integration of audiovisual in- causal inference of the neuroplastic effects (10). NEUROSCIENCE formation, whereas musicians rely mostly on the corresponding au- A recent fMRI study by Lee and Noppeney (11) investigated ditory information. The large-scale cortical network underpinning how sensorimotor experience molds temporal binding of auditory multisensory integration is reorganized due to expertise in a cogni- and visual signals. The results of this study indicated that musicians tive domain that largely involves audiovisual integration, indicating exhibited increased audiovisual asynchrony responses and in- long-term training-related neuroplasticity. creased connectivity selectively for music, and not for speech, in a superior temporal sulcus–premotor–cerebellar circuitry that was functional connectivity | MEG | multisensory integration | cortical defined and constrained by the corresponding fMRI activation plasticity | musical training results. Nevertheless, larger scale connectivity networks underpin- ning multisensory perception still remain undiscovered. ultisensory integration is of such importance for our un- The goal of the present study was to investigate the functional Mderstanding of the surrounding world that its cortical cor- connectivity of the cortical network underpinning audiovisual relates interact with most of the neocortical regions, including the ones traditionally considered as unisensory (1). The cortical areas Significance that are usually referred to as multisensory include the superior temporal sulcus, the intraparietal sulcus, and the frontal cortex (2). Multisensory integration engages distributed cortical areas and is Nevertheless, recent evidence suggests that multisensory percep- thought to emerge from their dynamic interplay. Nevertheless, tion engages more widespread areas than what the classic modular large-scale cortical networks underpinning audiovisual perception approaches have so far assumed (1). Moreover, audiovisual in- have remained undiscovered. The present study uses magneto- tegration emerges from a dynamic interplay of distributed regions encephalography and a methodological approach to perform operating in large-scale networks (3). whole-brain connectivity analysis and reveals, for the first The amount of shared information within these large-scale net- time to our knowledge, the cortical network related to multi- works of distributed neuronal groups conceptualizes the notion of sensory perception. The long-term training-related reorganiza- functional connectivity (4). Recent methodological advances allow tion of this network was investigated by comparing musicians the identification of networks that emerge from whole-brain analyses to nonmusicians. Results indicate that nonmusicians rely on of neuroimaging data such as functional magnetic resonance imaging processing visual clues for the integration of audiovisual in- (fMRI) and magnetoencephalography (MEG) (5) and provide fer- formation, whereas musicians use a denser cortical network that tile ground for studying the functional connectivity patterns of higher relies mostly on the corresponding auditory information. These cognitive processes. These kinds of networks are modeled as graphs data provide strong evidence that cortical connectivity is reor- composed of nodes, which represent the cortical areas contributing ganized due to expertise in a relevant cognitive domain, in- to the network, and by edges, which represent the connections be- dicating training-related neuroplasticity. tween the nodes. Each network has specific attributes that quantify connectivity organization (6). These graphs depict the functional Author contributions: E.P., A.K., S.C.H., P.D.B., and C.P. designed research; E.P. performed research; E.P. contributed new reagents/analytic tools; E.P. analyzed data; and E.P., A.K., connectome of the respective cognitive processes. Recent evidence S.C.H., P.D.B., and C.P. wrote the paper. suggests that functional connectivity networks may be reorganized by The authors declare no conflict of interest. factors mediating neuroplasticity such as learning and development This article is a PNAS Direct Submission. J.P.R. is a guest editor invited by the Editorial (7), altering information processing pathways. Board. Music notation reading encapsulates auditory, visual, and 1To whom correspondence should be addressed. Email: [email protected]. motor information in a highly organized manner and therefore This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. provides a useful model for studying multisensory phenomena 1073/pnas.1510662112/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1510662112 PNAS Early Edition | 1of6 Downloaded by guest on September 24, 2021 Fig. 1. Paradigm of an audiovisual congruent and incongruent trial. (A) A congruent trial. (B) An incongruent trial. The line “time” represents the duration of the presentation of the auditory and visual part of the stimulus. The last picture of each trial represents the intertrial stimulus in which subjects had to answer if the trial was congruent or incongruent. integration, and particularly the identification of abstract audiovi- network of sources (P < 0.001; FDR corrected) compiled from 62 sual incongruences. Additionally, we aimed to address how this edges and 62 nodes, connecting mainly occipital (7 sources), pari- network is reorganized due to learning and whether expertise in a etal (12 sources), temporal (12 sources), and frontal (22 sources) cognitive domain that largely involves audiovisual integration, such areas (Fig. 2). In contrast to the musicians’ network, the non- as music reading, may relate to changes in whole-brain functional musicians’ network was lateralized mainly toward the left hemi- connectivity. To this aim we used MEG to measure the cortical sphere. The global efficiency of the network was found to be E = connectivity of a group of musicians and a group of musically naïve 0.00041, the density of the network was found to be D = 0.00016, controls to congruent and incongruent audiovisual stimuli (Fig. 1). whereas the node strength identified that the node with the greatest Source analysis was performed using a realistic head model to solve sum of strengths was located in the left middle frontal gyrus. the forward problem and standardized low resolution electromag- The between-groups comparison revealed that the congruent > netic tomography (sLORETA) (12) to solve the inverse one. The incongruent network of the musicians differed significantly (P < source time series were analyzed in terms of their underlying con- 0.001; FDR corrected) from the one of nonmusicians, showing nectivity, by measuring their mutual information (MI) and apply- greater connectivity in a network compiled from 68 edges and 49 ing a statistical model to extract the significant connections of the nodes, mainly connecting temporal (17 sources) and frontal network. This approach allowed us
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